Pharmacology Glaucoma

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Pharmacological and environmental factors

in primary angle-closure glaucoma

Ian Subak-Sharpe, Sancy Low, Winifred Nolan, and Paul J. Foster*

Moorfields Eye Hospital, London, UK; UCL Institute of Ophthalmology, London, UK,andBirmingham and Midland Eye Centre, Birmingham, UK

Introduction or background: A large number of drug classes have now been

reported to provoke angle closure in high-risk individuals. The mechanism of

action can be generalized into three main categories: sympathomimetic,

parasympatholytic and idiosyndratic reactions.

Sources of data: This review of the ophthalmic literature provides a clinical

summary of primary angle-closure glaucoma (PACG) and its management.

Areas of agreement: External stimuli (pharmacological and environmental) may

induce acute, and more often, asymptomatic angle closure, which carries a

significant risk of glaucoma.

Growing points: Whenever in doubt, patients at risk of PACG who are starting

on drug therapy known to provoke angle closure or aggravate the condition

should be referred for detailed gonioscopic examination of the anterior

chamber by an ophthalmologist.

Areas for developing research: The use of new imaging methods such as

anterior segment optical coherence tomography to assess the presence or risk of

angle closure is gaining popularity, and may offer a more rapid method of

identifying people who are at risk of sight loss from angle-closure glaucoma

precipitated by non-ophthalmological medication.

Keywords: angle-closure/glaucoma/drugs/environment

Background

Glaucoma is the worlds commonest cause of irreversible blindness,currently affecting 60 million people with 8.4 million blind, and pro-jected to rise to 80 million by 2020 with 11.2 million blind.1 It is anoptic neuropathy associated with characteristic cupping of the opticdisc and progressive visual field loss. In the disease, the retinal ganglioncell axons are damaged as they enter and transit through the optic disc.The pathophysiology of the condition is attributed to either directpressure, causing a block of axoplasmic flow, or indirect reduction in

British Medical Bulletin 2010; 93: 125143

DOI:10.1093/bmb/ldp042

& The Author 2009. Published by Oxford University Press. All rights reserved.

For Permissions, please e-mail: [email protected]

Accepted: October 13,

2009

*Correspondence to:

P. Foster, Department of

Epidemiology and

Molecular Genetics, UCL

Institute of

Ophthalmology, 11-43

Bath Street, London EC1V

9EL, UK. E-mail: p.foster@

ucl.ac.uk

Published Online November 17, 2009


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optic nerve head blood flow, caused by a lowering of the vascular per-fusion pressure.2 However, the balance between these two mechanismsis often unclear.

For clinical purposes, glaucoma is normally classified according tothe presence or absence of obstruction by the iris to the outflow

pathway of aqueous humour at the level of the proximal trabecularmeshwork in the anterior chamber drainage angle (the angle betweenthe peripheral cornea and the iris). Such cases are referred to as angle-closure glaucoma and open-angle glaucoma, respectively. While theprevalence of primary open-angle glaucoma is greater than primaryangle-closure glaucoma (PACG) in the Western world, the primaryangle closure accounts for 50% of global glaucoma blindness.1

There are three conceptual stages in the natural history of PACG.Initially, contact between the peripheral iris and the trabecular mesh-work occurs with no clinically discernable impact on the intraocularpressure (IOP) or the tissues of the trabecular meshwork. These casesare termed anatomically narrow angle or primary angle-closure sus-pects. In many cases, this progresses to the formation of adhesionsbetween iris and trabecular meshwork, or an increase in the IOP. Thisstage is termed primary angle closure and denotes an establisheddisease. Unless promptly and effectively managed, the condition mayprogress to cause glaucomatous optic neuropathy, or PACG, whichcauses significant functional impairment of the vision.3

The clinical course through these conceptual stages can be acute(indicating a rapid onset of extremely high IOP causing symptoms ofpain, redness and reduced vision) or chronic (indicating an asympto-

matic course). Most textbooks and review articles that accounts forPACG emphasize the presence of symptoms as a defining feature ofacute angle closure (AAC). When treated promptly and effectively,acute cases (Fig. 1) can usually be prevented from developing glauco-matous optic neuropathy or significant visual deficits3 However, angleclosure often follows an asymptomatic course, referred to as chronicangle closure. Eyes with the asymptomatic (chronic) form of thedisease typically present late to medical services often with advancedglaucomatous damage and visual field loss. From population-basedresearch in the high-risk populations of Asia, it appears that more than

50% of cases of angle-closure glaucoma remain asymptomatic untilthere is profound loss of vision in the later stages.47 Despite earlytreatment, some patients who initially present with acute symptoms,will progress to develop chronic angle-closure glaucoma. Hence, long-term follow-up may be required for some patients after AAC.

Angle closure in Europe is less common. In the AAC register atMoorfields Eye Hospital serving Greater London, an average of onecase per week presents to eye casualty with the condition (personal

I. Subak-Sharpe et al.

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communication, D. Siriwardena). In the Rotterdam eye study, 2% ofan unselected population aged 55 years and over had a narrow anteriorchamber angle at risk of closure on examination of the limbalchamber depth. This was twice as high in women as men.8 In theEgna-Neumarkt study in Northern Italy, angle-closure glaucoma wasfound in 0.6% of the population, accounting for a quarter of all theglaucoma cases.

Drugs and poisons, both therapeutic and recreational, as well asenvironmental factors have been linked to the development of angleclosure in susceptible patients. These often present with symptoms, but

may have a chronic insidious course leading to PACG. Best currentevidence does not support the use of a classification system focused onsymptomatology to describe PACG.9 This review is focused on thedrug and environmental mechanisms that may trigger angle closureand lead to glaucomatous optic neuropathy if left untreated. It willallow the reader to identify patients at risk and understand the ration-ale behind the treatment of these cases.10

Diagnostic provocation of the occludable angle

The use of eye drops (pilocarpine and phenylephrine together) to assessa narrow angle that may be at risk of occluding and predispose apatient to PACG is known as the Mapstone provocative test.11 Therationale of the Mapstone test is that simultaneous contraction of thesphincter and dilator muscles of the iris in opposite directions leads topupil-block angle closure (Fig. 2), triggering elevated IOP in an at-riskeye. Alternatively, more physiological stimuli may be used: the

Fig. 1 An eye with AAC, with clinical signs of a mid-dilated pupil, hazy cornea and injected

blood vessels (courtesy of medical illustrations, Moorfields Eye Hospital).

Angle-closure glaucoma and systemic medication

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darkroom test12 or prone-position test13 may be performed by eitherplacing the patient in a darkroom or a prone-position for 6090 min. Ifthe peripheral iris obstructs the trabecular meshwork and leads to IOPelevation of 8 mmHg or more, this is considered a positive result. Thesetwo tests can be combined in the darkroom prone-position test.14,15

Pharmacological mydriasis/dilation of the pupil with topical phenyl-ephrine (sympathomimetic), atropine and cyclopentolate (both anticholi-nergic parasympatholytics) can precipitate angle closure due to crowdingof the peripheral iris in the fully dilated state (Fig. 3). There may be a lag

Fig. 3 (A) This figure demonstrates a normal but narrow angle before pupil dilation. The

peripheral iris is thick but the trabecular meshwork (TM) is visible for the sector of the eye

in this illustration. (B) After pupillary dilation, there is marked crowding of the peripheral

iris and occlusion of the drainage angle.

Fig. 2 (A) Normal anterior chamber angle anatomy: the trabecular meshwork (TM) is

found at the angle between the iris and the cornea, and constitutes the main drainage

structure that removes aqueous humour (AH) from the eye. AH is produced by the ciliary

body (CB), passing through the space between the iris and the lens into the anterior

chamber, finally draining out of the eye from the TM. (B) In pupil-block angle closure, AH

is unable to pass through the anterior chamber due to the pupillary sphincter being adher-

ent to the anterior lens (curved arrows). A positive force in the posterior chamber due toAH build-up (vertical arrows) leads to a rise in IOP, and blockage of the TM and anterior

chamber angle (illustrations for Figs 24 are courtesy of Mr Alan Lacey).


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of 14 h before the onset of symptoms secondary to significantly raisedIOP. Resolution of pharmacological dilation can also precipitate AACthrough pupil-block in a similar way to the Mapstone provocative testmentioned above (Fig. 2).

Apart from topical sympathomimetic or anticholinergic eye drops,angle closure has now been reported in many classes of drugs, some ofwhich affect autonomic function and may result in permanent visualloss and glaucomatous optic neuropathy. The patients most at risk ofdeveloping angle closure are typically older, female patients withshallow anterior chambers. They are often, but not invariably, hyper-metropic and have bulky crystalline lenses. In younger people, an ana-tomical predisposition known as plateau iris may be present16

(Fig. 4). Plateau iris may be associated with multiple ciliary bodycysts.17 Clinical features to look out for in the high-risk eye are pre-sented in Table 1.

Mechanisms of drug-induced angle closure

There are several different mechanisms that may cause iridotrabecular

contact, and result in pathological angle closure. These mechanisms aretypically described as acting at four distinct anatomical locations, eachprogressively more posterior: the pupil margin, the peripheral iris, thecilio-lenticular space and retro-lenticular potential space. Pupil-block(Fig. 2) occurs as a result of a differential pressure gradient fromthe posterior segment where the aqueous humour is formed andthe anterior chamber where the fluid is drained. Pupil-block mayalso occur in the presence of peripheral iris crowding or plateau iris.

Fig. 4 (A) This figure demonstrates a normal and wide-open angle. (B) In contrast to (A),

this diagram shows a particular iris configuration known as plateau iris, which occurs in

younger patients, where the peripheral iris makes a sharp angulation at the drainage

angle, causing it to be blocked. The central iris profile is flat, compared with the mechan-

ism illustrated in Fig. 2b.


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The latter two can lead directly to iris obstruction of the trabecularmeshwork and subsequent angle closure.

Drug-induced angle closure is the result of: (1) crowding of theanterior chamber angle as a result of pupillary dilation, (2) pupil-blockas the dilated pupil constricts or (3) idiosyncratic drug reactions thatchange the irido-corneal angle by formation of cilio-choroidal effusions(Fig. 5). Table 2 gives a list of the drug classes and mechanisms ofaction. The important drug classes that have been associated withangle closure are now discussed individually.

Bronchodilators

Asthma and chronic obstructive airway disease are frequently treatedwith bronchodilator medications. These are usually either a2adrenergicagonists or anticholinergics. Nebulized forms of ipratropiumbromide,18,19 atropine20 and salbutamol (albuterol)21 used on their own

Fig. 5 This is an UBM image of a patient with drug-induced angle closure, the iris is

pressed against the anterior chamber angle and the CB is rotated anteriorly. The uveoscl-

eral effusion (*) seen here is typical of the idiosyncratic mechanism of adverse reactions

that precipitate AAC (courtesy of Mr Gus Gazzard).

Table 1: The high-risk eye.

Individual risk factors

Age Age of 60 years or older is a major risk factor for AAC, relative risk 9.1 in

Singapore.

Gender AAC affects women two to four times as often as men, irrespective of race.

Cataracts Bulky cataracts are associated with pupil-block and peripheral iris crowding.

Race Chinese race found to be a relative risk of 2 2.8 in Singapore; 11.8% of AlaskanEskimo women over 60 years was found to have occludable angles.

Family history A positive family history has been observed in cases of PACG.

Ocular risk factors

Refraction Patients with angleclosure are more likely to be hypermetropic than myopic.

Axial biometry Shorter anterior chamber depths and axial length are demonstrated in patients

with occludable angles than in normal controls.

Plateau iris Approximately 50% of patients under 40 years had plateau iris.


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have each provoked AAC. However, most patients suffering an acuteasthma attack receive combinations of these medications often in highdoses, as nebulized preparations. AAC has been reported on a number ofoccasions for the combination of nebulized ipratropium bromide withsalbutamol.2225 The route of absorption of these agents into the eye isunclear. However, it has been suggested that nebulized administration ofthese medications allows a significant dose to be absorbed over the con-junctiva and cornea. To avoid this, it has been suggested that patientscould be fitted with goggles, or the holes in the sides of mask, which

discharge vapour across the cornea, could be occluded.

Antidepressants

The major classes of antidepressants that cause angle closure are tri-cyclic antidepressants (TCAs) and serotonin-specific reuptake inhibitors(SSRIs).2628 TCAs have historically been associated with a high inci-dence of anticholinergic (muscarinic) side-effects such as dry mouthand constipation. Newer tricyclic-related drugs such as trazodone have

a lesser side-effect profile. AAC has been widely reported amongpatients using clomipramine29 and imipramine, a less sedative tricyclic.30

Although trazodone has less anticholinergic (muscarinic) side-effectsthan the older tricyclics, chronic low dose use in a patient known tohave PACG resulted in poor IOP control during trazodone use.31

SSRI were originally developed and promoted for their lack of seda-tion or systemic antimuscarinic side-effects. They are now the mostwidely used antidepressants in the UK. However, they do have

Table 2: Drug provoked angle closure by mechanisms of action and drug classes.

Sympathomimetic activity

b2-Agonists Salbutamol (albuterol), ritodrine

a-Agonists Phenylephrine

Nasal decongestants Phenylpropanolamine

Cocaine

Anticholinergic activity

TCA Imipramine, clomipramine, trazadone

SSRIs Paroxetine, citalopram, fluvoxamine, venlafaxine

Muscarinic antagonists Oxybutynin, atropine, botulinum toxin A, tropicamide

Other drug classes (idiosyncratic reactions)

Antihistamine Promethazine

Amphetamines Ecstasy

Sulpha-containing drugs Sulphamethoxazole, trimethoprim, acetazolamide

Thiazide diuretic Hydrochlorthiazide

Antiepileptic Topiramate

Antidepressant Escitalopram


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anticholinergic properties and several of the SSRIs have been shown tohave the potential to provoke symptomatic AAC either at therapeuticdosage or in overdose. Paroxetine has been the SSRI most frequentlyreported in this context3235 with patients ranging widely in age andduration of time from initiating treatment to onset of angle-closure

symptoms.Of the other SSRIs, both citalopram36 and escitalopram37 have been

reported to be associated with AAC. The mechanism of angle closurefor escitalopram was through production of a ciliochoroidal effusion(Fig. 5), ciliary body detachment and rotation of the iris and anteriorchamber angle.37 This was diagnosed before any glaucomatous discdamage and resolved after topical cycloplegics and discontinuation ofthe escitalopram. Fluvoxamine, another SSRI has been implicated inprovoking AAC in a patient known to have narrow angles and glau-coma. The patients symptoms were reversed upon stopping themedication.38

Venlafaxine is a serotonin and noradrenaline re-uptake inhibitor,widely used for depression as it is thought to have less sedative andantimuscarinic effects than the tricyclics. It is also used to treat irritablebowel syndrome, where it is thought to act both by modulating centraland peripheral sensory mechanisms and by reducing associateddepression. However, there have now been several reports of AAC withvenlafaxine via an idiosyncratic mechanism with supraciliary effu-sions.3941 It remains unclear whether this is due to serotoninergiceffects, anticholinergic effects or weak adrenergic effects.

Serotinergic agents are also used as appetite suppressants and dexfen-

fluramine prescribed for this has been associated with AAC by inducingpupil-block.42

Anticholinergics given for urinary incontinence and as antispasmodics

Over active bladder (OAB) and detrusor instability are extremelycommon conditions, affecting one in three of those over 75 years old.43

The involuntary bladder contractions, mediated by muscarinic recep-tors in the detrusor muscle, occur during the bladder filling phase. The

mainstay of treatment for OAB is anticholinergic medication.Symptomatic AAC has been reported in an 80-year-old hypermetropetaking oxybutynin for urge incontinence.44 The British NationalFormulary lists glaucoma as a contraindication to use of anticholiner-gics for these conditions, although it makes no distinction betweenopen-angle glaucoma and angle-closure glaucoma, nor betweenpatients who have had previous laser treatment for their occludableanterior chamber angles. The risk of angle closure is reduced but not


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eradicated by laser iridotomy. These patients are therefore consideredto be at lower (but not negligible) risk.45

General anaesthetics

Patients undergoing general anaesthesia procedures are often givenintravenous anticholinergic medications such as atropine to preventside-effects from neostigmine, a reversible cholinesterase inhibitor usedat the end of operation to reverse non-depolarizing muscle relaxants.Although small doses of parenteral atropine were found not to producemydriasis, larger doses did, especially in lightly pigmented eyes.46

There have been several case series of patients suffering AAC aftergeneral anaesthesia47,48 and have resulted in permanent visual lossfrom glaucomatous optic neuropathy. Atropine is sometimes usedafter coronary angioplasty, and a case of AAC after this has beenrecorded.49

Over-the-counter medicines and cough suppressants

Phenylephrine has marked a1-adrenergic properties and is frequentlyused by eye care professionals to produce mydriasis (pupil dilation) fordiagnostic and therapeutic purposes. It is also a common constituent ofmany over-the-counter cold remedies and is also used to treat epistaxis,by direct intranasal application to produce vasoconstriction, usually

prior to nasal packing or cautery. Its use has been associated withAAC, when given nasally for epistaxis,50 and as part of anover-the-counter medicine Fenox nasal drops (PhenylephrineHydrochloride BP 0.5% w/v with Cetrimide Ph Eur, Glycerin Ph Eur,Methylhydroxybenzoate Ph Eur).51 The phenomenon of phenylephrine-induced angle closure is not infrequently seen in oph-thalmology clinics after topical (eyedrop) application, for fundal exam-ination. Mydriatic-induced angle closure is used in glaucoma clinics,after peripheral iridotomy, as a test to assess safety and determine ifthere is a need of long-term pilocarpine prophylaxis.

Many over-the-counter cold and cough remedies contain constituents,included as antihistamines or decongestants, which also have markedsympathomimetic or anticholinergic effects. AAC has been reported ina patient after taking the recommended dose of Night Nurse, whichcontains the antihistamine promethiazine, and Day Nurse (GlaxoSmithkline) which contains the decongestant phenylpropanolamine.52

These ingredients are far from unique to these products though: pro-methazine is a component of Medised, Phenergan, Tixylix Night-time,


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Avomine, Pamergan, Sominex, Ronpiron, Phensedyl, Phenhalal and QMazine: Phenylpropanolamine is also found in Contac 400, VicksColdcare, Mu-cron, Benylin Day and Night, Allereze, Dimotapp,Nirolex prolonged release, Sinutab, Triogesic and Triominic.52 In astudy from Hong Kong, up to 25% of cases that present with AAC had

recently taken antitussive medication that precipitated the event.53

Recreational drugs

Cocaine hydrochloride causes pupil dilation due to its adrenergic prop-erties. It is often given medically to reduce bleeding, particularly fromthe nasal mucosa. Acute angle closure has been reported after cocaineapplication intranasally during dacryocystorhinostomy surgery54 andafter elective antral washout.55 AAC has also been reported after ipsi-lateral intranasal cocaine abuse.56

In contrast to cocaine, methylenedioxymethamphetamine (ecstasy) isonly used recreationally. Bilateral AAC was reported in a youngwoman who used ecstasy and marijuana.57 No choroidal effusionswere found. However in another case report of a young man whonoticed progressive decrease in vision after taking ecstasy for 2 weekswas found to have choroidal effusions and transient myopia whichresolved upon cessation of the drug.58

Botulinum toxinBotulinum toxin inhibits the release of acetylcholine and could theor-etically cause mydriasis. A case of AAC has been recorded shortly aftertreatment of blepharospasm with botulinum toxin.59

Other sympathomimetics

Ritodrine is a direct acting sympathomimetic drug, predominantly ab2-agonist, which is used to reduce uterine contractions and stop pre-

mature labour. It is usually given by intravenous infusion. BilateralAAC has been reported 8 h after starting a ritodrine infusion for pre-mature labour.60 However, labour itself has also been implicated intriggering AAC.61

There has been a case report of angle closure developing a few hoursafter ingestion of sildenafil (Viagra).62 However, angle closure has alsobeen associated with sexual activity63 and the drug may not actually bethe association in this case.64


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preceding period.81 In Singapore,84 there was a direct relationshipbetween symptomatic angle closure and both number of sunspots andmean solar radio flux. Increased sunspot activity is associated with asmall increase in solar radiation, terrestrial geomagnetic storms andheating of the Earths outer atmosphere.84 It remains unclear whether

sunspot activity is truly associated with AAC.

Adrenaline and stress

Two 73-year old sisters presented with simultaneous AAC after havingbeen involved in a fight with each other.86 The release of adrenalineduring the squabble, and associated mydriasis, was thought to be thecausative factor.

AAC has been reported a number of times after eyelid surgery, in par-ticular blepharoplasty.8789 These cases were thought to have beencaused by adrenaline-induced angle closure (several millilitres of localanaesthetic-containing adrenaline is injected for haemostasis) in eyeswith coexistent occludable anterior chamber angles.

Identification of cases and management

The current reference-standard of angle width assessment is gonio-scopy, in which the anterior chamber angle is examined using a diag-nostic contact lens. Other screening techniques include the obliqueflashlight test, van Herick technique at the slit lamp microscope andnewer imaging techniques including high-resolution ultrasound biomi-croscopy (UBM) and optical coherence tomography (OCT) of theanterior segment. Some of these imaging techniques are not widelyavailable (see also Figs 5 and 6).

Management of angle closure

Laser iridotomy

The creation of a full thickness hole in the peripheral iris using laser(previously argon laser but now superseded by either combined argonand Nd:YAG laser, or YAG laser alone) is termed an iridotomy.90,91

Prior to the development of laser technology this hole was made bysurgical means (surgical iridectomy). The iridotomy allows the aqueoushumor to bypass the pupil to eliminate any pupil-block mechanism ofangle closure. Iridotomy is implemented at diagnosis in all patientswith acute or established primary angle closure. Itis often used as


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a preventive treatment in patients with iridotrabecular contact, particu-larly in cases that need frequent pupil dilation for retinal examinations(e.g. diabetics). It is, however, less effective where extensive areas ofperipheral anterior synechiae already exist causing permanent angleclosure.

Iridoplasty

Peripheral iridotomy is the usual first-line treatment of patients withAAC. A significant number of patients have evidence of residual appo-sitional angle-closure post-iridotomy. In some of these cases low-powerArgon laser burns are applied to the peripheral iris to contract it awayfrom the trabecular meshwork thereby opening the angle.9294

Iridoplasty may also be used as initial treatment for patients in AAC.Once angle closure has been overcome, a peripheral laser iridotomy isperformed.

Lens extraction

For patients with a co-existing cataract and angle closure, removing thelens by surgical means will also have a therapeutic effect on the angle-closure process.95 In many patients with chronic angle closure, thisachieves adequate control of the IOP.96

Medical treatment

Cholinergic agents, such as pilocarpine, can be delivered as eye drops.These cause constriction of the pupil and thus pull the peripheral irisaway from the trabecular meshwork, opening the drainage angle.

Other topical and systemic IOP lowering medications are usually givento help control IOP in AAC and may help control IOP in chronicangleclosure.

Discussion and conclusion

Most cases of primary angle closure probably occur in patients forwhom there are no identifiable, exogenous causative agents. However,environmental and pharmacological factors (both systemic and topical)

can cause angle closure and glaucomatous optic neuropathy if leftuntreated. This review draws from a very large number of case reports.The message is that patients do not always have typical textbookaccounts of acute symptomatic or chronic asymptomatic presenta-tions of angle closure. All healthcare professionals should be aware ofthe risks of angle closure from certain systemic medications, in predis-posed individuals. Referral to an ophthalmologist for gonioscopyshould be arranged whenever there is any doubt.


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It seems anomalous that current drug guidelines potentially depriveall glaucoma patients of beneficial medications, when most have a typeof glaucoma (either open-angle or treated angle closure) which will notbe aggravated by their use. There remains a lack of understandingabout the difference between angle-closure and open-angle glaucoma.97

Instead of using a blanket recommendation contraindicating the use ofthese medications for all glaucoma patients, one option is to assessthem for closable angles prior to giving medications that mightproduce angle closure. Ideally, patients that have been identified to beat high risk (see Table 1) should be assessed prior to starting treatment.However, this may not be practical to implement, even in populationswith high prevalence of angle closure.

Clinicians should ensure that all patients understand that they needto seek urgent ophthalmic attention should they develop blurred vision,or a red or painful eye, after starting any one of these medications. Allpatients over the age of 40 years, and those with a positive familyhistory of glaucoma should undergo regular examination by an opto-metrist or ophthalmologist.

Acknowledgements

The views expressed in this publication are those of the authors andnot necessarily those of the Department of Health.

Funding

The authors acknowledge (a proportion of their) financial supportfrom the Department of Health through the award made by theNational Institute for Health Research to Moorfields Eye HospitalNHS Foundation Trust and UCL Institute of Ophthalmology for aSpecialist Biomedical Research Centre for Ophthalmology.

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